Floral Induction Process Research Articles

Abiotic and biotic factors regulate the timing of floral induction: a review

AbstractTime of flowering is an important phenomenon which ensures reproductive success and better adaptability to various environmental conditions. There are a few proteins that function as master regulators of flowering. The expression of these proteins highly depends on many extrinsic and intrinsic factors along with several biotic components. Further, alterations in these factors result in drastic changes in the transition from the vegetative to the reproductive phase that ultimately results in yield loss. Different abiotic stresses, such as drought, salinity, cold, heat, nutrient scarcity, sugar availability and exogenous chemicals, collectively affect the whole ambit of the floral induction process. Nevertheless, biotic stresses like bacterial (Pseudomonas syringae) and fungal (Fusarium oxysporum) infections promote the expression of the FT gene, which further accelerates the flowering phenomenon. Soil‐dwelling microorganisms, herbivores, pollinators and a few endophytes are associated with the promotion of flowering. Although plants have adapted several strategies to cope with the stress conditions and manage to maintain their reproductive physiology, it is noteworthy that flowering in plants under stress conditions shows species‐specific response patterns by accelerating or retarding the floral induction. Several transcription factors and some miRNAs were also involved in the regulation of flowering under stress conditions. In this review, we have summarised the different biotic and abiotic stresses that affect the flowering time and also include several strategies that plants adapt to escape the stress condition.

Evolutionary assessment of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in citrus relatives with a specific focus on flowering

Phase transition and floral induction in citrus requires several years of juvenility after germination. Such a long period of juvenility has been a major hindrance to its genetic improvement program. Studies have shown that miR156 along with its downstream genes SQUAMOSA PROMOTER BINDING PROTEINS (SBP) and SBP-LIKE (SPL) mediate the phase transition and floral induction process in plants. Our current study has systematically analyzed SPLs in 15 different citrus-related species, systematically annotated them based on their close homology to their respective Arabidopsis orthologs, and confirmed the functional attributes of the selected members in floral precocity. The majority of the species harbored 15 SPLs. Their cis-element assessment suggested the involvement of the SPLs in diverse developmental and physiological processes in response to different biotic and abiotic cues. Among all, SPL5, SPL9, and SPL11 stood out as consistently differentially expressed SPLs in the adult and young tissues of different citrus-related species. Independent overexpression of their F. hindsii orthologs (FhSPL5, FhSPL9, and FhSPL11) brought an enhanced expression of endogenous FLOWERING LOCUS T leading to the significantly precocious flowering in transgenic Arabidopsis lines. Future study of the genes in the citrus plant itself is expected to conclude the assessments made in the current study.Graphical

Rootstock-mediated carbohydrate metabolism, nutrient contents, and physiological modifications in regular and alternate mango (Mangifera indica L.) scion varieties.

Most of the popular scion varieties of mango possess alternate/irregular bearing. There are many external and internal factors assigned, among them carbohydrate reserves, and nutrient content plays important roles in the floral induction process in many crop species. In addition to that rootstock can alter the carbohydrate reserve and nutrient acquisition of scion varieties in fruit crops. The present investigation was carried out to understand the effect of rootstocks on the physiochemical traits of leaf, and bud and nutrient content in regular and alternate bearing varieties of mango. The rootstock "Kurukkan" promoted starch content in leaves of both alternate bearing varieties 'Dashehari' (5.62 mg/g) and regular 'Amrapali' (5.49 mg/g) and encouraged higher protein content (6.71 mg/g) and C/N ratio (37.94) in buds of alternate bearing 'Dashehari'. While Olour rootstock upregulated the reducing sugar in leaves of 'Amrapali' (43.56 mg/g) and promoted K (1.34%) and B (78.58 ppm) content in reproductive buds of 'Dashehari'. Stomatal density in 'Dashehari' scion variety was found higher on Olour rootstock (700.40/mm 2), while the rootstock fails to modify stomatal density in the scion variety regular bearer 'Amrapali'. Further, a total of 30 carbohydrate metabolism-specific primers were designed and validated in 15 scion/rootstock combinations. A total of 33 alleles were amplified among carbohydrate metabolism-specific markers, which varied from 2 to 3 alleles with a mean of 2.53 per locus. Maximum and minimum PIC value was found for NMSPS10, and NMTPS9 primers (0.58). Cluster analysis revealed that scion grafted on Kurukkan rootstock clustered together except 'Pusa Arunima' on Olour rootstock. Our analysis revealed that Fe is the key component that is commonly expressed in both leaf and bud. Although Stomatal density (SD) and Intercellular CO2 Concentration (Ci) are more specific to leaf and Fe, B, and total sugar (TS) are abundant in buds. Based on the results it can be inferred that the physiochemical and nutrient responses of mango scion varieties are manipulated by the rootstock, hence, the scion-rootstock combination can be an important consideration in mango for selecting suitable rootstock for alternate/irregular bearer varieties.

Genome-Wide Identification and Expression Analyses of CONSTANS-Like Family Genes in Cucumber (Cucumis sativus L.)

The CONSTANS-like (COL) gene family is one of the plant-specific transcription factor families that play important roles in plant growth and development. However, the knowledge of COLs related in cucumber is limited, and their biological functions, especially in the photoperiod-dependent flowering process, are still unclear. In this study, twelve CsaCOL genes were identified in the cucumber genome. Phylogenetic and conserved motif analyses provided insights into the evolutionary relationship between the CsaCOLs. Further, the comparative genome analysis revealed that COL genes are conserved in different plant species, especially collinearity gene pairs related to CsaCOL5. Ten kinds of cis-acting elements were vividly detected in CsaCOLs promoter regions, including five light-responsive elements, which echo the diurnal rhythm expression patterns of seven CsaCOL genes under SD and LD photoperiod regimes. Combined with the expression data of developmental stage, three CsaCOL genes are involved in the flowering network and play pivotal roles for the floral induction process. Our results provide useful information for further elucidating the structural characteristics, expression patterns, and biological functions of COL family genes in many plants

HD-ZIP I Transcription Factor (PtHB13) Negatively Regulates Citrus Flowering through Binding to FLOWERING LOCUS C Promoter.

For floral induction in adult citrus, low temperature is one of the most important environmental factors. FLOWERING LOCUS C (FLC) plays a very important role in low-temperature-induced Arabidopsis flowering by repressed FLC expression under exposure to prolonged low-temperature conditions. However, little is known about the FLC regulation mechanism in perennial woody plants such as citrus. In this study, the functions of citrus FLC homolog (PtFLC) were investigated by ectopic expression in Arabidopsis. Transcription factor of homeodomain leucine zipper I (HD-ZIP I) as an upstream regulator of PtFLC was identified by yeast one-hybrid screen to regulate its transcription. The HD-ZIP I transcription factor was highly homologous to Arabidopsis ATHB13 and thus was named PtHB13. Ectopically expressed PtHB13 inhibited flowering in transgenic Arabidopsis. Furthermore, the expression of PtFLC and PtHB13 showed a seasonal change during the floral induction period and was also affected by low temperature. Thus, we propose that PtHB13 binds to PtFLC promoter to regulate its activity during the citrus floral induction process.

Effect of exogenous spermidine on floral induction, endogenous polyamine and hormone production, and expression of related genes in \u2018Fuji\u2019 apple (Malus domestica Borkh.)

Flower bud formation in ‘Fuji’ apple (Malus domestica Borkh.) is difficult, which severely constrains commercial production. Spermidine (Spd) plays an important role in floral induction, but the mechanism of its action is incompletely understood. To investigate the effect of Spd on flowering, 6-year-old ‘Fuji’ apple trees were treated with 1 × 10−5 mol L−1 Spd to study the responses of polyamines [putrescine (Put), Spd and spermine (Spm)], hormones [gibberellins (GA3) and abscisic acid (ABA)], and polyamine-, hormone- and flowering-related genes. Spd application promoted flowering during floral induction by increasing MdGA2ox2 (gibberellin 2-oxidase) through GA3 reduction and increasing MdNCED1 and MdNCED3 (9-cis-epoxycarotenoid dioxygenase) through ABA enrichment during 60 to 80 days after full bloom. The flowering rate as well as the expressions of flower-related genes, except for MdLEY (LEAFY), also increased, thereby promoting flowering. In addition, spraying with Spd significantly increased the contents of endogenous polyamines except for Spm in terminal buds by increasing the expressions of polyamine-associated genes. We hypothesize that the contribution of Spd to flowering is related to crosstalk among polyamines, hormone signals, and related gene expressions, which suggests that Spd participates in the apple floral induction process.

Ethylene synthesis in mango ‘Palmer’ production

Ethylene is an important hormone in the floral induction process of the mango tree. However, climatic conditions such as the high temperatures that occur in the Brazilian semi-arid can raise the levels of ethylene and cause abortion of flowers and fruits, impairing the production. Thus, the goal of this study was to evaluate the effect of the ethylene biosynthesis inhibitor complex (Ni, Co and Mo) on flowering and ‘Palmer’ mango production. The experiment was set up in a randomized block design with six treatments and four replications. The treatments were five increasing levels of the commercial product Profol NiCoMo Dry® (Ni: 2.4%, Co: 1.2% and Mo: 26%) at concentrations of 0.25, 0.50, 0.75, 1.00 and 1.25 g L(‑1) and a control, in a volume of 800 L ha(‑1), at pre-flowering. Three weekly applications were carried out, starting with the second application of nitrate for floral induction. Evaluations were made for the number and length of panicles; number of fruits branch(‑1) of the sun rising side (NFRN), of the west side (NFRP) and total (NFR); length, diameter and fruit mass. The increase in the levels of Profol NiCoMo Dry up to 1.25 g L(‑1) promoted a linear increase in panicle length, fruit set and total number of fruit plant‑1, resulting in a linear reduction of fruit size (mass), without compromising the commercial standard. Increasing levels of Profol NiCoMo Dry up to 1.25 g L(‑1) promoted a cubic response in fruit yield, with the lowest obtained (23.30 t ha‑1) when using 0.1 g L(‑1) and the maximum (36.20 t ha(‑1)) for the level of 1.23 g L(‑1).

De novo Transcriptome Assembly of Floral Buds of Pineapple and Identification of Differentially Expressed Genes in Response to Ethephon Induction.

A remarkable characteristic of pineapple is its ability to undergo floral induction in response to external ethylene stimulation. However, little information is available regarding the molecular mechanism underlying this process. In this study, the differentially expressed genes (DEGs) in plants exposed to 1.80 mL·L−1 (T1) or 2.40 mL·L−1 ethephon (T2) compared with Ct plants (control, cleaning water) were identified using RNA-seq and gene expression profiling. Illumina sequencing generated 65,825,224 high-quality reads that were assembled into 129,594 unigenes with an average sequence length of 1173 bp. Of these unigenes, 24,775 were assigned to specific KEGG pathways, of which metabolic pathways and biosynthesis of secondary metabolites were the most highly represented. Gene Ontology (GO) analysis of the annotated unigenes revealed that the majority were involved in metabolic and cellular processes, cell and cell part, catalytic activity and binding. Gene expression profiling analysis revealed 3788, 3062, and 758 DEGs in the comparisons of T1 with Ct, T2 with Ct, and T2 with T1, respectively. GO analysis indicated that these DEGs were predominantly annotated to metabolic and cellular processes, cell and cell part, catalytic activity, and binding. KEGG pathway analysis revealed the enrichment of several important pathways among the DEGs, including metabolic pathways, biosynthesis of secondary metabolites and plant hormone signal transduction. Thirteen DEGs were identified as candidate genes associated with the process of floral induction by ethephon, including three ERF-like genes, one ETR-like gene, one LTI-like gene, one FT-like gene, one VRN1-like gene, three FRI-like genes, one AP1-like gene, one CAL-like gene, and one AG-like gene. qPCR analysis indicated that the changes in the expression of these 13 candidate genes were consistent with the alterations in the corresponding RPKM values, confirming the accuracy and credibility of the RNA-seq and gene expression profiling results. Ethephon-mediated induction likely mimics the process of vernalization in the floral transition in pineapple by increasing LTI, FT, and VRN1 expression and promoting the up-regulation of floral meristem identity genes involved in flower development. The candidate genes screened can be used in investigations of the molecular mechanisms of the flowering pathway and of various other biological mechanisms in pineapple.

Putative sugarcane FT/TFL1 genes delay flowering time and alter reproductive architecture in Arabidopsis.

Agriculturally important grasses such as rice, maize, and sugarcane are evolutionarily distant from Arabidopsis, yet some components of the floral induction process are highly conserved. Flowering in sugarcane is an important factor that negatively affects cane yield and reduces sugar/ethanol production from this important perennial bioenergy crop. Comparative studies have facilitated the identification and characterization of putative orthologs of key flowering time genes in sugarcane, a complex polyploid plant whose genome has yet to be sequenced completely. Using this approach we identified phosphatidylethanolamine-binding protein (PEBP) gene family members in sugarcane that are similar to the archetypical FT and TFL1 genes of Arabidopsis that play an essential role in controlling the transition from vegetative to reproductive growth. Expression analysis of ScTFL1, which falls into the TFL1-clade of floral repressors, showed transcripts in developing leaves surrounding the shoot apex but not at the apex itself. ScFT1 was detected in immature leaves and apical regions of vegetatively growing plants and, after the floral transition, expression also occurred in mature leaves. Ectopic over-expression of ScTFL1 in Arabidopsis caused delayed flowering in Arabidopsis, as might be expected for a gene related to TFL1. In addition, lines with the latest flowering phenotype exhibited aerial rosette formation. Unexpectedly, over-expression of ScFT1, which has greatest similarity to the florigen-encoding FT, also caused a delay in flowering. This preliminary analysis of divergent sugarcane FT and TFL1 gene family members from Saccharum spp. suggests that their expression patterns and roles in the floral transition has diverged from the predicted role of similar PEBP family members.

Changes in CsFT Transcript Abundance at the Onset of Low-temperature Floral Induction in Sweet Orange

As in arabidopsis (Arabidopsis thaliana), putative citrus (Citrus) Flowering locus T (FT) homologs are strong promoters of flowering and apparently are key components of the molecular mechanism controlling floral induction in these species. An abundance of citrus FT gene transcripts during floral induction is consistent with the role of their products as floral-promoting signals. However, specific details about how the floral induction process is initiated and sustained remain largely unknown. We report changes in transcript abundance of a FT gene (CsFT) from sweet orange (Citrus sinensis) at the onset of floral induction by low temperatures and at different times of the day. Using a combination of field and growth room experiments, we determined that the abundance of CsFT transcripts increased within 1 day after initial exposure to cool floral-inductive temperatures, and that CsFT transcript abundance was higher in the afternoon than in the morning and evening. The presence of photoperiod cycles seemed to be required to sustain the increasing CsFT transcript abundance, because exposure to floral inductive conditions under continuous light or darkness did not increase the abundance of CsFT transcripts after 3 days. Our results suggest that the regulation of CsFT expression responds rapidly (overnight) to the onset of floral-inductive cool temperatures, is sensitive to changes in temperature, and requires alternation of light and dark cycles to sustain transcript accumulation during induction.

Floral induction (FI) in longan ( Dimocarpus longan, Lour.) trees: Part I. Low temperature and potassium chlorate effects on FI and hormonal changes exerted in terminal buds and sub-apical tissue

Floral induction (FI) in longan ( Dimocarpus longan, Lour.) trees was achieved in controlled greenhouse experiments by low temperature (LT) and by the application of potassium chlorate at high temperature (HT + KClO 3) during two consecutive seasons. The latter treatment was successful also at temperatures above 20 °C. The present experiment was conducted to investigate possible alterations in the concentrations of plant hormones exerted by these two methods and to relate them to the floral induction process. The following hormones were examined by radioimmunoassay in the shoot apical buds (SAB), and in sub-apical bark and wood: the auxin indole-3-acetic acid (IAA); gibberellins (GAs); and the cytokinins zeatin/zeatin riboside (Z/ZR) and isopentenyl-adenine/isopentenyl-adenosine (iP/iPA). In apical buds, the LT treatments initially increased gibberellin and auxin (IAA) concentrations, which later declined significantly as compared to the non-inductive HT control treatment. Campared to the LT treatment the influence of HT + KClO 3 on GA 3 and IAA concentrations were less clear. On the other hand this treatment clearly increased the cytokinins Z/ZR and to some extend also the iP/iPA content in the apical bud. In both sub-apical wood and bark CKs were increased. The study found that hormonal changes induced by LT and HT + KClO 3 in apical buds and in sub-apical tissue were different for GAs and IAA on the one hand and CKs on the other. It is speculated that LT and HT + KClO 3 induce floral induction in longan at least partially by different hormonal reactions.

Immunohistochemical localization of IAA and ABP1 in strawberry shoot apexes during floral induction

By using an anti-indole-acetic acid (anti-IAA) monoclonal antibody and an anti-auxin-binding protein 1 (anti-ABP1) polyclonal antibody, IAA and ABP1 were immunohistochemically localized in strawberry (Fragaria ananassa Duch.) shoot apexes during floral induction. The spatial distribution patterns of endogenous IAA and ABP1 and their dynamic changes during floral induction were investigated. In addition, the affect of 1-N-naphthylphtalamic acid (NPA) on IAA distribution during floral induction was also analyzed. The results showed that IAA was present in the shoot apexes throughout the floral induction process, gradually concentrating in the shoot apical meristem (SAM). The distribution of ABP1 and its dynamic changes were similar to those of IAA. In addition, the ABP1 immune signal in SAM gradually increased as floral induction developed. On a morphological level, these results indicate both the spatial distribution and dynamic changes in endogenous IAA and ABP1 during the floral induction process. The close correlation found between IAA and ABP1 indicates that a cooperation occurs during the regulation of floral induction. The results also suggest that IAA was the significant agent for floral induction, and that SAM might be the place of the main action. Treatment with NPA during floral induction prevented the accumulation of IAA in the SAM, delayed the process of floral differentiation and induced an abnormal flower development. It is likely that IAA in the shoot apex is produced in young leaves and transported through the vascular tissues to the SAM and other places of function. Finally, an appropriate amount of IAA in the SAM and normal polar auxin transport are essential for floral induction and differentiation in strawberries.

Effect of winter chilling and paclobutrazol on floral bud production in Eucalyptus nitens

Flower bud production of Eucalyptus nitens is comparatively abundant at specific high altitude sites in the South African summer rainfall region. This suggests that cumulative cold may be implicated in the floral induction process. Therefore, three chill models were used to investigate whether winter temperature data can be related to E. nitens flower bud production at sites differing in chill accumulation. Amount of accumulated winter chill, in conjunction with paclobutrazol treatment, was able to explain between 66 and 72% of the variation in E. nitens flower bud production. Although the potential chilling requirement of E. nitens can be calculated with similar accuracy by each of the chill models tested, the Dynamic Model performed best under the particular range of experimental conditions. At low to moderate levels of winter chill (43 to 81 Chilling Portions (CPs) of the Dynamic Model), paclobutrazol application hastened first flowering and increased the percentage reproductive trees by between 5–27% in the case of seedlings, and between 2–62% in the case of grafts. At high levels of winter chill (> 87 CPs), paclobutrazol had a negligible effect on the percentage reproductive trees in the case of either seedlings or grafts. At four and five years after planting, very high levels of accumulated winter chill (96 CPs) stimulated a high percentage of seedlings (25–50%) and grafts (55–64%) to produce flower buds. Considerable variation in precocity and chilling requirement (for floral induction) is evident within the South African E. nitens breeding population. A better accuracy in relating E. nitens floral bud production to amount of prior winter chilling could be achieved by further experimentation involving fewer genotypes and a wider range of chilling conditions.

LEAFY expression and flower initiation in Arabidopsis.

During the initial vegetative phase, the Arabidopsis shoot meristem produces leaves with associated lateral shoots at its flanks, while the later reproductive phase is characterized by the formation of flowers. The LEAFY gene is an important element of the transition from the vegetative to the reproductive phase, as LEAFY is both necessary and sufficient for the initiation of individual flowers. We have analyzed in detail the expression of LEAFY during the plant life cycle, and found that LEAFY is extensively expressed during the vegetative phase. In long days, Arabidopsis plants flower soon after germination, and this is paralleled by rapid upregulation of LEAFY. In short days, Arabidopsis plants flower several weeks later than in long days, but LEAFY expression increases gradually before flowering commences. Application of the plant hormone gibberellin, which hastens flowering in short days, enhances the gradual change in LEAFY expression observed in short days. Changes in LEAFY expression before the transition to flowering suggest that the time point of this transition is at least partly controlled by the levels of LEAFY activity that are prevalent at a given time of the life cycle. This assumption is borne out by the finding that increasing the copy number of endogenous LEAFY reduces the number of leaves produced before the first flower is formed. Thus, LEAFY combines properties of flowering-time and flower-meristem-identity genes, indicating that LEAFY is a direct link between the global process of floral induction and the regional events associated with the initiation of individual flowers.

Illuminating flowers: CONSTANS induces LEAFY expression.

Higher plants must undergo a major developmental switch, the transition to flowering, if they are to successfully complete their life cycle. In many plants, the crucial decision of when to begin to produce flowers is primarily controlled by environmental signals. The process of floral induction involves the integration of the activities of two types of genes: those that control flowering time as a response to the environment as well as an endogenous clock, and those that determine the floral identity of the cells. The first direct link between these two classes of genes has now been demonstrated. Forced expression of CONSTANS, a flowering-time gene, promotes flowering through the transcriptional activation of LEAFY, a flower-meristem-identity gene.

Floral Induction in Growing Buds of Lychee (Litchi chinensis) and Mango (Mangifera indica)

Buds of potted plants of the terminal flowering tree species lychee (Litchi chinensis) and mango (Mangifera indica) forced to begin growth at high temperatures (florally non-inductive) and then transferred to low temperatures produced inflorescences, so the whole process of floral induction can occur in growing buds. Floral initials were visible in lychee within 39 days of transfer to low temperature and 30 days in mango, indicating that floral induction occurs relatively quickly in both species. In most cases where plants were transferred to winter ambient temperatures for floral induction, pre-activated (growing) buds flowered more consistently than buds that were dormant at the time of transfer. If the buds were small when plants were transferred from high temperature to low temperature, leafless inflorescences formed. If buds were a little larger, leafy inflorescences formed, with leaves basally and flowers terminally. If the buds were larger again, the shoots were purely vegetative. All these observations are consistent with floral induction occuning while the bud is growing and provide for much improved experimental systems for studying the physiology of floral induction in species such as lychee and mango.

Analysis of the role of the late‐flowering locus, GI, in the flowering of Arabidopsis thaliana

SummaryThe mutation gigantea (gi) is recessive and belongs to the late‐flowering mutations in Arabidopsis thaliana. The late‐flowering mutations result in a pronounced delay in flowering due to a prolonged phase of vegetative growth, which is manifested by an increased number of primary foliage leaves in the rosette (i.e. vegetative nodes). To examine the nature of the gi mutation, detailed phenotypic analysis was carried out for three representative mutant alleles. The results indicate that gi mutants have a defect in the promotion of the floral induction process by long‐day photoperiods and not in the flowering process per se. Temperature‐shift experiments using a partially conditional allele were employed to determine the timing of the functional requirement for the product of the GI locus. The end of the deduced functional period corresponds to the period at which transition of the apical meristem from the vegetative to the reproductive phase occurs. Such timing is in good agreement with the postulated role of the GI locus. These results demonstrate that the GI locus is involved in the promotion of floral initiation (entrance of the meristem into the transitional stage) by long‐day photoperiods.

Effect of glutathione and alloxan on the photoperiodic response of Xanthium.

IT has been recently reported by Brachet1 that a morphogenetic process in the alga Acetabularia is promoted by a substance containing —SS— and that the same process is inhibited by substances containing —SH. It appeared of interest, therefore, to test the morphogenetic responses of higher plants to substances containing thiol groups. For this purpose the effect of reduced glutathione on the process of floral induction in Xanthium, a short-day plant, was investigated. Alloxan, on the other hand, was chosen as an agent known to reduce rapidly the content of reduced glutathione of blood by both oxidation and coupling reactions2,3.